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Two Theobroma cacao genotypes with contrasting pathogen tolerance show aberrant transcriptional and ROS responses after salicylic acid treatment.

ABSTRACT: Understanding the genetic basis of pathogen susceptibility in various crop plants is crucial to increasing the stability of food, feed, and fuel production. Varietal differences in defence responses provide insights into the mechanisms of resistance and are a key resource for plant breeders. To explore the role of salicylic acid in the regulation of defence in cacao, we demonstrated that SA treatment decreased susceptibility to a pod rot pathogen, Phytophthora tropicalis in two genotypes, Scavina 6 and Imperial College Selection 1, which differ in their resistance to several agriculturally important pathogens. Transient overexpression of TcNPR1, a major transcriptional regulator of the SA-dependent plant immune system, also increased pathogen tolerance in cacao leaves. To explore further the genetic basis of resistance in cacao, we used microarrays to measure gene expression profiles after salicylic acid (SA) treatment in these two cacao genotypes. The two genotypes displayed distinct transcriptional responses to SA. Unexpectedly, the expression profile of the susceptible genotype ICS1 included a larger number of pathogenesis-related genes that were induced by SA at 24h after treatment, whereas genes encoding many chloroplast and mitochondrial proteins implicated in reactive oxygen species production were up-regulated in the resistant genotype, Sca6. Sca6 accumulated significantly more superoxide at 24h after treatment of leaves with SA. These experiments revealed critical insights regarding the molecular differences between cacao varieties, which will allow a better understanding of defence mechanisms to help guide breeding programmes.

SUBMITTER: Fister AS

PROVIDER: S-EPMC4588882 | biostudies-literature | 2015 Oct

REPOSITORIES: biostudies-literature

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Two Theobroma cacao genotypes with contrasting pathogen tolerance show aberrant transcriptional and ROS responses after salicylic acid treatment.

Fister Andrew S AS O'Neil Shawn T ST Shi Zi Z Zhang Yufan Y Tyler Brett M BM Guiltinan Mark J MJ Maximova Siela N SN

Journal of experimental botany 20150710 20

Understanding the genetic basis of pathogen susceptibility in various crop plants is crucial to increasing the stability of food, feed, and fuel production. Varietal differences in defence responses provide insights into the mechanisms of resistance and are a key resource for plant breeders. To explore the role of salicylic acid in the regulation of defence in cacao, we demonstrated that SA treatment decreased susceptibility to a pod rot pathogen, Phytophthora tropicalis in two genotypes, Scavin ...[more]

PMID: 26163705

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Project description:BackgroundThe pathogenesis-related (PR) group of proteins are operationally defined as polypeptides that increase in concentration in plant tissues upon contact with a pathogen. To date, 17 classes of highly divergent proteins have been described that act through multiple mechanisms of pathogen resistance. Characterizing these families in cacao, an economically important tree crop, and comparing the families to those in other species, is an important step in understanding cacao's immune response.ResultsUsing publically available resources, all members of the 17 recognized pathogenesis-related gene families in the genome of Theobroma cacao were identified and annotated resulting in a set of ~350 members in both published cacao genomes. Approximately 50 % of these genes are organized in tandem arrays scattered throughout the genome. This feature was observed in five additional plant taxa (three dicots and two monocots), suggesting that tandem duplication has played an important role in the evolution of the PR genes in higher plants. Expression profiling captured the dynamics and complexity of PR genes expression at basal levels and after induction by two cacao pathogens (the oomycete, Phytophthora palmivora, and the fungus, Colletotrichum theobromicola), identifying specific genes within families that are more responsive to pathogen challenge. Subsequent qRT-PCR validated the induction of several PR-1, PR-3, PR-4, and PR-10 family members, with greater than 1000 fold induction detected for specific genes.ConclusionsWe describe candidate genes that are likely to be involved in cacao's defense against Phytophthora and Colletotrichum infection and could be potentially useful for marker-assisted selection for breeding of disease resistant cacao varieties. The data presented here, along with existing cacao-omics resources, will enable targeted functional genetic screening of defense genes likely to play critical functions in cacao's defense against its pathogens.

Project description:BACKGROUND:Witches' broom disease (WBD) of cacao (Theobroma cacao L.), caused by Moniliophthora perniciosa, is the most important limiting factor for the cacao production in Brazil. Hence, the development of cacao genotypes with durable resistance is the key challenge for control the disease. Proteomic methods are often used to study the interactions between hosts and pathogens, therefore helping classical plant breeding projects on the development of resistant genotypes. The present study compared the proteomic alterations between two cacao genotypes standard for WBD resistance and susceptibility, in response to M. perniciosa infection at 72 h and 45 days post-inoculation; respectively the very early stages of the biotrophic and necrotrophic stages of the cacao x M. perniciosa interaction. RESULTS:A total of 554 proteins were identified, being 246 in the susceptible Catongo and 308 in the resistant TSH1188 genotypes. The identified proteins were involved mainly in metabolism, energy, defense and oxidative stress. The resistant genotype showed more expressed proteins with more variability associated with stress and defense, while the susceptible genotype exhibited more repressed proteins. Among these proteins, stand out pathogenesis related proteins (PRs), oxidative stress regulation related proteins, and trypsin inhibitors. Interaction networks were predicted, and a complex protein-protein interaction was observed. Some proteins showed a high number of interactions, suggesting that those proteins may function as cross-talkers between these biological functions. CONCLUSIONS:We present the first study reporting the proteomic alterations of resistant and susceptible genotypes in the T. cacao x M. perniciosa pathosystem. The important altered proteins identified in the present study are related to key biologic functions in resistance, such as oxidative stress, especially in the resistant genotype TSH1188, that showed a strong mechanism of detoxification. Also, the positive regulation of defense and stress proteins were more evident in this genotype. Proteins with significant roles against fungal plant pathogens, such as chitinases, trypsin inhibitors and PR 5 were also identified, and they may be good resistance markers. Finally, important biological functions, such as stress and defense, photosynthesis, oxidative stress and carbohydrate metabolism were differentially impacted with M. perniciosa infection in each genotype.

Project description:Grafting typically offers a shortcut to breed tree orchards throughout a multidimensional space of traits. Despite an overwhelming spectrum of rootstock-mediated effects on scion traits observed across several species, the exact nature and mechanisms underlying the rootstock-mediated effects on scion traits in cacao (Theobroma cacao L.) plants often remain overlooked. Therefore, we aimed to explicitly quantify rootstock-mediated genetic contributions in recombinant juvenile cacao plants across target traits, specifically cadmium (Cd) uptake, and its correlation with growth and physiological traits. Content of chloroplast pigments, fluorescence of chlorophyll a, leaf gas exchange, nutrient uptake, and plant biomass were examined across ungrafted saplings and target rootstock × scion combinations in soils with contrasting levels of Cd. This panel considered a total of 320 progenies from open-pollinated half-sib families and reciprocal full-sib progenies (derived from controlled crosses between the reference genotypes IMC67 and PA121). Both family types were used as rootstocks in grafts with two commercial clones (ICS95 and CCN51) commonly grown in Colombia. A pedigree-based best linear unbiased prediction (A-BLUP) mixed model was implemented to quantify rootstock-mediated narrow-sense heritability (h 2) for target traits. A Cd effect measured on rootstocks before grafting was observed in plant biomass, nutrient uptake, and content of chloroplast pigments. After grafting, damage to the Photosystem II (PSII) was also evident in some rootstock × scion combinations. Differences in the specific combining ability for Cd uptake were mostly detected in ungrafted rootstocks, or 2 months after grafting with the clonal CCN51 scion. Moderate rootstock effects (h 2> 0.1) were detected before grafting for five growth traits, four nutrient uptake properties, and chlorophylls and carotenoids content (h 2 = 0.19, 95% CI 0.05-0.61, r = 0.7). Such rootstock effects faded (h 2< 0.1) when rootstock genotypes were examined in soils without Cd, or 4 months after grafting. These results suggest a pervasive genetic conflict between the rootstock and the scion genotypes, involving the triple rootstock × scion × soil interaction when it refers to Cd and nutrient uptake, early growth, and photosynthetic process in juvenile cacao plants. Overall, deepening on these findings will harness early breeding schemes of cacao rootstock genotypes compatible with commercial clonal scions and adapted to soils enriched with toxic levels of Cd.

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Two Theobroma cacao genotypes with contrasting pathogen tolerance show aberrant transcriptional and ROS responses after salicylic acid treatment.

Publications

Two Theobroma cacao genotypes with contrasting pathogen tolerance show aberrant transcriptional and ROS responses after salicylic acid treatment.

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